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The role of ultraviolet-B from sun exposure on vitamin D3 and parathyroid


hormone level in elderly women in Indonesia

Article · January 2008

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Asian J Gerontol Geriatr 2007; 2: 126–32

The role of ultraviolet-B from ORIGINAL ARTICLE


sun exposure on vitamin D3 and
parathyroid hormone level in elderly
women in Indonesia
S Setiati1 MD, PhD, M Oemardi2 MD, B Sutrisna3 MD, PhD,
Supartondo4 MD

ABSTRACT 1
Division of Geriatric, Department of
Internal Medicine, School of Medicine,
Objectives. To assess the effect of ultraviolet-B (UVB) from sun University of Indonesia, Indonesia
exposure on vitamin D3 [25(OH)D] status and parathyroid hormone 2
Division of Endocrine Metabolic,
Department of Internal Medicine, School
(PTH) concentration in elderly Indonesian women. of Medicine, University of Indonesia,
Methods. A total of 74 elderly women were randomised into the Indonesia
3
Faculty of Public Health, University of
intervention group (receiving UVB from sun exposure at 0.6 minimal Indonesia, Indonesia
erythemal dose/hour on the face and both arms 3 times a week for 6 weeks 4
Division of Geriatric, Department of
plus calcium carbonate 1000 mg per day) and a control group (receiving Internal Medicine, School of Medicine,
University of Indonesia, Indonesia
only calcium carbonate 1000 mg per day). Main outcome measures were
25(OH)D, PTH, and serum calcium levels at weeks 0 and 6.
Results. The prevalence of 25(OH)D deficiency was 35%. In the
intervention group, the mean 25(OH)D concentration increased from
59 nmol/L to 84 nmol/L, but increased only slightly in the control group.
There was no change of PTH levels in either group. In the intervention
subgroup with deficient serum levels of 25(OH)D, post-intervention
levels increased markedly, but PTH levels decreased only slightly.
Conclusion. Ultraviolet B from sun exposure for 25 minutes, 3 times a Correspondence to: Dr S Setiati, Division of
week for 6 weeks improves the vitamin D status, but not the PTH levels. Geriatric, Department of Internal Medicine,
Faculty of Medicine, University of Indonesia,
Jl. Diponegoro no.71, Jakarta 10430,
Key words: Aged; Parathyroid hormone; Sunlight; Ultraviolet rays; Indonesia. E-mail: s_setiati@plasa.com,
Vitamin D s_setiati@yahoo.com

INTRODUCTION vitamin D deficiency is related to lower muscle


strength, increased body sway and falls.13-17 Several
Vitamin D is important for proper development factors contribute to vitamin D deficiency in elderly
and maintenance of serum calcium levels, skeletal women, including: decreased vitamin D synthesis in
integrity, vascular health, and cancer prevention.1-3 the skin, reduced metabolic activity in the liver and
The hormonal form of vitamin D [1,25 (OH)2D3] kidney, diminished sun exposure, and lower vitamin
acts through a nuclear receptor with many functions, D intake.18-22
including calcium and phosphate absorption in the
intestine, calcium mobilisation in bone, and calcium Vitamin D deficiency in the elderly population
reabsorption in the kidney, all of which maintain can be treated by supplementing vitamin D (orally or
calcium homeostasis and bone mineralisation in the by injection) or increasing vitamin D synthesis with
body.4-7 ultraviolet (UV) irradiation using artificial ultraviolet-
B (UVB) or sun exposure. Most studies to date have
Vitamin D deficiency leads to secondary entailed vitamin D supplementation and artificial
hyperparathyroidism, increased bone turnover, UV irradiation.23-26 Only a few studies have reported
bone loss, and is also implicated as a cause of hip the effect of sun exposure as a means of increasing
fracture.8-12 Furthermore, in the elderly population, vitamin D3 [25(OH)D].27,28 Whether UVB from

126 Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007


Sun exposure on vitamin D3 and parathyroid level

sun exposure in equatorial countries can increase defined as a level of >69 pg/mL. Before the study, all
25(OH)D and decrease parathyroid hormone (PTH) four research assistants received training regarding
concentration among elderly women was the question all necessary procedures as well as the study protocol.
we posed. Our study population in Indonesia had Sample size was determined based on the confidence
the following features: type-4 brown skin, old age, interval of 95%, a study power of 90%, and assuming
low body mass index, and physiological changes in an effect size of 20%. A total of 80 elderly subjects
many organ systems related to vitamin D synthesis. were recruited.
It was reported that 7-dehydrocholesterol in the skin
was reduced due to the ageing process.19,29 Another The study entailed two stages. In the first stage,
question to resolve was the proper extent of sun the intensity of UVB from sun exposure was measured
exposure time necessary. Thus, the aim of our study in the randomly selected institutionalised care units
was to obtain the dosage of additional sun exposure in Jakarta and Bekasi, where the study was being
(in terms of intensity and duration) necessary to yield carried out. Measurement of sun exposure intensity
a measurable difference in 25(OH)D and PTH levels was performed daily, every hour, from 7 am to 4 pm,
in elderly Indonesian women. over 7 consecutive days . The minimal erythemal
dose (MED)/hour as recorded by the UV meter was
METHODS noted and a mean value was calculated. The time and
duration of each exposure were based on the exposure
Ours was a randomised clinical trial with a parallel intensity calculated as above. In the second stage, 20
design, entailing additional UVB from deliberate subjects from each institutionalised care unit were
sun exposure as the intervention. The study was randomised to either an intervention or control group.
undertaken during the wet (rainy) season (February Those in the intervention group were trained to expose
to March 2006) on elderly women from four their face and both arms to sun for specified durations
randomly selected institutionalised care units (two at specified times, as defined in the first stage. The
were government run and two were privately run) in intervention was carried out 3 times a week for 6
two cities, Jakarta and Bekasi. weeks. Subjects were advised to carry out recreational
activities and wear sunglasses during each exposure,
All the subjects were elderly women (≥60 years) without application of sunscreen to their face and
who fulfilled the entry criteria (not bed ridden, willing arms. Subjects in the control group were trained to
to enter study, no liver abnormalities, kidney failure carry out corresponding activities indoors.
or skin cancers, and not in receipt of phenobarbitone
or phenytoin). Data pertaining to each subject Subjects in both groups were given calcium
(demographic characteristics, time and length of carbonate 2 x 500 mg per day during 6 weeks of
sun exposure, 25(OH)D, PTH and serum calcium observation. They were questioned in terms of
levels, nutrient intake [calorie, protein, fat, calcium, outdoor activities, as well as about the frequency and
and vitamin D], height, weight, and skin type) duration of such activities before entering the study.
were collected. A UV meter (UV meter model 7.0, Data on each subject’s nutrient intake were collected
Solartech, US) was used to measure UVB intensity before and during the study, based on 24-hour food
from sun exposure, a microtoise and a weighing scale recall and food weighing (performed by dietitians).
to measure height and weight. A mexameter was Serum 25(OH)D, PTH, and calcium levels were
used to obtain the melanin index (for skin type), and measured before and 6 weeks after sun exposure.
food recall and food record questionnaires to collect
nutritional information. Levels of 25(OH)D and PTH Data were analysed using Stata (version 8.0).
were measured by enzyme-linked immunosorbent Mean values for MED/hour in the first stage was
assay30,31 performed in an internationally standardised calculated to determine the exact dose for sun
(ISO 9001) clinical laboratory. As the latter two exposure. t-Test for paired samples were used
molecules are very unstable at room temperature, to compare the difference of 25(OH)D and PTH
the blood samples were kept in the freezer at -20ºC levels before and after the intervention. t-Tests for
to prevent underestimation before measurement. independent samples were used to compare the
Vitamin D deficiency was defined as a 25(OH)D difference of 25(OH)D and PTH levels after 6 weeks
level of <50 nmol/L. Increased PTH level was in the exposed (intervention) and unexposed groups.

Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007 127


Setiati et al

Table 1
Mean minimal erythemal dose (MED) per hour at the selected institutionalised care
units

Time Mean MED/hour


West Jakarta North Jakarta South Jakarta Bekasi
07.00 0.1 0.1 0.2 0.4
08.00 0.2 0.4 0.4 0.5
09.00 0.6 0.7 0.7 0.6
10.00 0.8 1.2 1.1 0.8
11.00 1.3 1.4 1.8 1.2
12.00 1.1 1.7 2.3 1.6
13.00 0.8 1.3 2.1 1.8
14.00 0.6 0.9 1.3 1.2
15.00 0.2 0.6 0.6 0.4
16.00 0.1 0.5 0.3 0.4

Any p values of <0.05 denoted statistical significance (p>0.05) or the frequency of being outdoors and
using two-tailed tests. the duration of sun exposure (p>0.05). Before
intervention, 26 (35%) of the subjects had 25(OH)D
RESULTS deficiency and/or an elevated PTH concentration.

The lowest intensity of sun exposure was obtained at After 6 weeks of sun exposure, the mean
7 am. The intensity increased rapidly until 11 am, after 25(OH)D concentration increased significantly
which it stabilised somewhat but reached maximum (p<0.001). Mean values and percentage differences
at 2 pm (Table 1). According to Holick,4 the simplest of 25(OH)D concentration before and after this
way to obtain vitamin D from sun exposure was by period were significantly higher in the intervention
exposing face, arms, and hands for a period equal to group than in the controls (p=0.01). The mean
25% of the time that it would take to cause 1 MED. In 25(OH)D and PTH concentrations before and after 6
this stud­y, the highest intensity (more or less 2 MED/ weeks of sun exposure are shown in Table 3. Before
hour) occurred at 11 am to 1 pm. Thus it took only ¼ commencement, the mean 25(OH)D concentration
x 60 minutes/2 = 7.5 minutes to increase 25(OH)D in the intervention group was lower in older than
concentration. It transpired that high UVB intensity younger subjects; the mean percentage change was
(heat of sunlight) at 11 am to 1 pm caused patients also greater in those who were older.
inconvenience and decreased their compliance. The
preferred time for sun exposure was at 9 am, when For further analysis, subjects were divided into
the UVB intensity was 0.6 MED/hour, meaning that it those with normal and deficient 25(OH)D concen-
took 25 minutes (¼ x 1 MED/0.6 MED x 60 minutes) trations. Table 4 shows that in the intervention group,
for each exposure. All subjects in the intervention 25(OH)D concentration increased significantly, and
group then received 25 minutes for each exposure, 3 more so in the deficient than normal group (77% vs
times a week for 6 weeks. 32%). In the deficient group, the PTH level decreased
1% after sun exposure but in the normal group it
The 80 subjects recruited consisted of 42 in the increased 11%. There was no statistically significant
intervention group and 38 controls. Six from the difference between those two groups (p=0.34).
former group were excluded from the analysis due Serum calcium levels increased significantly both in
to incomplete sun exposure. A total of 74 subjects the deficient and normal groups (both p<0.001). In
completed the study. Most (77%) of the subjects the control group, subjects with normal 25(OH)D
were aged 60 to 75 years and the rest were 76 to concentrations had an increase in their mean
90 years old. The characteristics of the subjects in 25(OH)D concentration after 6 weeks. In the deficient
the two groups are shown in Table 2. There were group, mean 25(OH)D concentration increased but
no statistically significant differences in this regard not to a statistically significant extent, and mean

128 Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007


Sun exposure on vitamin D3 and parathyroid level

Table 2
Demographic and lifestyle characteristics of subjects in the intervention and control groups before
treatment period*

Characteristic Intervention group (n=36) Control group (n=38) p Value


Age (years) 71±6 72±8 0.69†
Body mass index (kg/m ) 2
2±4 22±4 0.67†
Calcium ion (mmol/L) 1.09±0.03 1.10±0.04 0.12†
Vitamin D3: 25(OH)D (nmol/L) 59.1±20.4 64.8±21.5 0.25†
Parathyroid hormone (pg/mL) 62.9±2.6 58.5±2.1 0.43†
Calorie intake (Kcal) 1469±403 1500±399 0.74†
Protein intake (g) 34±9 35±9 0.69†
Calcium intake (mg) 254±8 242±10 0.59†
Vitamin D intake (µg) 20±8 20±15 0.79†
Outdoor frequency
Never 1 (3%) 5 (13%) 0.13‡
1/week 14 (39%) 19 (50%)
2-3/week 20 (56%) 12 (32%)
>3/week 1 (3%) 2 (5%)
Length of sun exposure per day (minutes)
None 1 (3%) 5 (13%) 0.19‡
<30 11 (31%) 14 (37%)
30-60 10 (28%) 11 (29%)
>60 14 (39%) 8 (21%)

* Data are shown in mean±SD or No. of patients (%)



Independent t-test

Chi squared test

Table 3
Mean vitamin D3 [25(OH)D], parathyroid hormone (PTH), and serum calcium concentrations before
and after 6-week treatment period

Variable Week 0 Week 6 Mean change (%) p Value (dependent


t-test)
Mean (SD)
25(OH)D (nmol/L)
Intervention group (n=36) 59.1 (20.4) 84.3 (21.2) +52 <0.001
Control group (n=38) 64.8 (21.5) 71.2 (23.2) +12 <0.001
p Value (independent t-test) 0.01 <0.001
PTH (pg/mL)
Intervention group (n=36) 62.9 (2.6) 64.5 (2.5) +7 0.62
Control group (n=38) 58.5 (2.1) 62.9 (2.7) +10 0.07
p Value (independent t-test) 0.82 0.65
Serum calcium (mmol/L)
Intervention group (n=36) 1.09 (0.03) 1.19 (0.04) +9 <0.001
Control group (n=38) 1.09 (0.04) 1.28 (0.09) +17 <0.001
p Value (independent t-test) <0.001

PTH levels increased from 70 to 79 pg/mL. 25(OH)D concentration were generally carried out in
white types-2 and -3 skin colour populations using
DISCUSSION artificial UVB.24-26 This is the first study to explore
the effect of UVB from sun exposure on 25(OH)D
Studies about the effect of UVB irradiation on and PTH levels in elderly women with type-4 skin.

Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007 129


Setiati et al

Table 4
Vitamin D3 [25(OH)D], parathyroid hormone (PTH), and calcium ion concentrations after treatment
period and percentage change from pre-treatment values

Variable Week 0 Week 6 Mean change (%) p Value (dependent


t-test)
Mean (SD)
Intervention group
25(OH)D (nmol/L)
25(OH)D normal (n=20) 74.9 (12.8) 96.6 (19.2) +32 <0.001
25(OH)D deficient (n=16) 39.4 (4.6) 68.8 (11.2) +77 <0.001
p Value (independent t-test) <0.001 <0.001
PTH (pg/mL)
25(OH)D normal (n=20) 53.3 (1.7) 57.3(1.7) +11 0.22
25(OH)D deficient (n=16) 76.1 (2.7) 74.1 (2.9) -1 0.74
p Value (independent t-test) 0.34 0.34
Calcium ion (mmol/L)
25(OH)D normal (n=20) 1.09 (0.02) 1.18 (0.04) +8 <0.001
25(OH)D deficient (n=16) 1.08 (0.03) 1.18 (0.04) +9 <0.001
p Value (independent t-test) 0.88 0.42
Control group
25(OH)D (nmol/L)
25(OH)D normal (n=20) 74.6 (15.7) 81.7 (16.2) +10 <0.001
25(OH)D deficient (n=16) 37.5 (6.1) 41.9 (11.7) +12 0.34
p Value (independent t-test) <0.001 0.54
PTH (pg/mL)
25(OH)D normal (n=20) 57.2 (21.5) 60.6 (23.3) +6 0.19
25(OH)D deficient (n=16) 70.0 (24.2) 79.1 (35.7) +13 0.14
p Value (independent t-test) 0.07 0.69
Calcium ion (mmol/L)
25(OH)D normal (n=20) 1.10 (0.04) 1.29 (0.09) +18 <0.001
25(OH)D deficient (n=16) 1.09 (0.03) 1.26 (0.07) +16 <0.001
p Value (independent t-test) 0.29 0.54

Since there were no data about the intensity of UVB important source, vitamin D status is expected
from sun exposure in tropical countries, especially to relate to geographic location, being better in
in Indonesia, the first stage of this study aimed to residents close to the equator compared to those at
obtain the MED/hour value in our randomly selected other latitudes. Vitamin D deficiency is thought to be
institutionalised care units, so as to determine the rare in the Indonesian population as the country is
time and duration of exposure the subjects might exposed to sunlight all year long. However, our study
need. This study encountered the highest intensity showed that the incidence of vitamin D deficiency
of UVB from sun exposure about 1 hour before in elderly women was high (35%). In other studies
and after midday. The exposure duration needed to of elderly housebound people and nursing home
increase 25(OH)D concentration was longer when residents, one quarter and one half respectively
subjects were exposed before 11 am and after 1 pm. were vitamin D deficient.10,32 Environmental factors
such as the frequency of outdoor activity, low levels
The lifestyle of most of the subjects in this study of sun exposure, and low dietary intake are likely
was healthy with regard to vitamin D status. They contributing factors to the high prevalence of vitamin
were not bed-ridden, undertook outdoor activities, D deficiency. The definition of vitamin D deficiency
and rarely used sunscreen, thus allowing enough may also affect estimation of its prevalence. However,
sun exposure. Given that sun exposure is the most our study was not designed to explore the risk factors

130 Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007


Sun exposure on vitamin D3 and parathyroid level

of vitamin D deficiency. Instead, our aim was to for the formation of enough 1.25(OH)2D3 needed to
measure the difference of 25(OH)D and PTH levels increase intestinal calcium absorption.
between exposed and non-exposed groups, before
and after sun enxposure. Other studies which used artificial UVB and
vitamin D supplementation found greater decreases
Data have consistently shown that in the healthy in PTH concentration.14,23 However, there are some
elderly people, 25(OH)D concentration is a function important differences between the study by Chel
of sun exposure. Cross-sectional and longitudinal et al23 and ours. Thus, all their subjects had severe
studies in white populations living in North Europe vitamin D deficiency (25(OH)D of <20 nmol/L) and
and North America exhibit a marked seasonal less skin pigmentation (type-2 and -3 skin). They also
variation in serum 25(OH)D concentration, being used artificial UVB exposure from a reliably stable and
lowest during winter months, and highest in late intense source.23 Both studies encountered the same
summer, consistent with the role of sun exposure phenomenon, namely the lower the pre-exposure
on 25 (OH)D concentrations.8,12,33 However, there 25(OH)D concentration, the greater the increase of
are certain other factors which also influence sun 25(OH)D concentration post-exposure.
exposure.34-36
Pfeifer et al14 compared elderly women given
Two demographic factors known to contribute to 1200 mg/day calcium and 800 IU/day vitamin
sun exposure are age and skin pigmentation. Ageing D supplementation for 8 weeks with those who
significantly affected the capacity of human skin to were given 1200 mg/day calcium supplementation
produce vitamin D.19 Ageing decreases the amount alone. They found that 25(OH)D increased 72%
of 7-dehydrocholesterol produced in the skin, by as and PTH decreased 18% in calcium and vitamin
much as 75% by the age of 70 years. Moreover, the D supplementation group. As in our study, they
increase in 25(OH)D concentrations is also lower in found that the 25(OH)D concentration increased
people who have greater amounts of melanin. The significantly more in the deficient group (77% vs
exposure of Caucasian subjects (type-2 and -3 skins) 72%).14 However, the PTH concentration decreased
with 1 MED artificial UV irradiation greatly increased less in our study than that in theirs (1.4% vs 18%).
25(OH)D concentrations by up to 60 fold within 24 Besides, the shorter duration of intervention (6
to 48 hours of exposure, whereas this dosage did weeks of sun exposure in our study vs 8 weeks
not significantly change 25(OH)D concentrations in of supplementation in theirs), as well as other
Black (type 5-6 skin) subjects.22 From the perspective differences in the two populations (kidney and
of vitamin D synthesis, our study showed that parathyroid gland function, race and ethnicity) may
skin photosynthesis and hydroxylation in the liver explain the contrasting PTH level responses.
performed well in Indonesian elderly women with
type-4 skin colour, which was expressed by significant The increase of 25(OH)D concentration after
increases of 25(OH)D concentration after 6 weeks of sun exposure indicated that our subjects achieved
sun exposure. good vitamin D synthesis in skin, although they
were elderly with type-4 skins. Further vitamin D
In the deficient group, PTH concentration synthesis in the liver was also good. Regrettably, the
decreased slightly (1.4%) after 6 weeks of sun increase of 25(OH)D concentration was not followed
exposure. This might have been due to better calcium by decreases in PTH concentration.
absorption after sun exposure (serum calcium levels
increased from 1.08 to 1.18 mmol/L) or the result of A limitation of our study was that the UV meter
calcium supplementation. In the deficient unexposed measures UVB as well as UVA. In the early morning
group, PTH concentration increased after 6 weeks more UVA gets through the stratosphere than UVB,
(70 to 79 pg/mL), although serum calcium levels and thus the total UVB we measured might have
increased from 1.09 to 1.26 mmol/L. From which it been a mix of both types.
may be assumed that the increase of serum calcium
levels was due to bone resorption through heightened In conclusion, vitamin D deficiency was found in
secondary hyperparathyroidism. Presumably, the low 35% of Indonesian elderly women in institutionalised
25(OH)D concentration in this group was insufficient care. Receipt of UVB from sun exposure for 25

Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007 131


Setiati et al

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132 Asian Journal of Gerontology & Geriatrics Vol 2 No 3 December 2007

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